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Alternative electron pathways of photosynthesis drive the algal CO2 concentrating mechanism

View ORCID ProfileAdrien Burlacot, View ORCID ProfileOusmane Dao, View ORCID ProfilePascaline Auroy, View ORCID ProfileStephan Cuiné, View ORCID ProfileYonghua Li-Beisson, View ORCID ProfileGilles Peltier
doi: https://doi.org/10.1101/2021.02.25.432959
Adrien Burlacot
Aix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint-Paul-lez-Durance, France
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  • ORCID record for Adrien Burlacot
Ousmane Dao
Aix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint-Paul-lez-Durance, France
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Pascaline Auroy
Aix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint-Paul-lez-Durance, France
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Stephan Cuiné
Aix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint-Paul-lez-Durance, France
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Yonghua Li-Beisson
Aix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint-Paul-lez-Durance, France
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Gilles Peltier
Aix Marseille Univ, CEA, CNRS, Institut de Biosciences et Biotechnologies Aix-Marseille, CEA Cadarache, 13108 Saint-Paul-lez-Durance, France
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  • ORCID record for Gilles Peltier
  • For correspondence: gilles.peltier@cea.fr
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Abstract

Global photosynthesis consumes ten times more CO2 than net anthropogenic emissions, and microalgae account for nearly half of this consumption1. The great efficiency of algal photosynthesis relies on a mechanism concentrating CO2 (CCM) at the catalytic site of the carboxylating enzyme RuBisCO, thus enhancing CO2 fixation2. While many cellular components involved in the transport and sequestration of inorganic carbon (Ci) have been uncovered3,4, the way microalgae supply energy to concentrate CO2 against a thermodynamic gradient remains elusive4-6. Here, by monitoring dissolved CO2 consumption, unidirectional O2 exchange and the chlorophyll fluorescence parameter NPQ in the green alga Chlamydomonas, we show that the complementary effects of cyclic electron flow and O2 photoreduction, respectively mediated by PGRL1 and flavodiiron proteins, generate the proton motive force (pmf) required by Ci transport across thylakoid membranes. We demonstrate that the trans-thylakoid pmf is used by bestrophin-like Ci transporters and further establish that a chloroplast-to-mitochondria electron flow contributes to energize non-thylakoid Ci transporters, most likely by supplying ATP. We propose an integrated view of the CCM energy supply network, describing how algal cells distribute photosynthesis energy to power different Ci transporters, thus paving the way to the transfer of a functional algal CCM in plants towards improving crop productivity.

One sentence summary Photosynthetic alternative electron flows and mitochondrial respiration drive the algal CO2 concentrating mechanism

Competing Interest Statement

The authors have declared no competing interest.

  • List of abbreviations

    BST
    Bestrophin-like proteins
    CCM
    Carbon Concentrating Mechanism
    CEF
    Cyclic Electron Flow
    Ci
    Inorganic Carbon
    CMEF
    Chloroplast-Mitochondria Electron Flow
    HLA3
    High Light Activated 3
    LCI
    Low Carbon Induced
    LEF
    Linear Electron Flow
    LHCSR3
    Light Harvesting Complex Stress Related 3
    Myxo
    Myxothiazol
    NPQ
    Non Photochemical Quenching
    PCEF
    Pseudo-Cyclic Electron Flow
    PGRL1
    Proton Gradient Regulation Like-1
    FLVs
    Flavodiiron proteins
    PSI
    Photosystem I
    PSII
    Photosystem II
    RuBisCO
    Ribulose Bisphosphate Carboxylase Oxygenase
    SHAM
    Salicyl hydroxamic acid.
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    Posted February 27, 2021.
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    Alternative electron pathways of photosynthesis drive the algal CO2 concentrating mechanism
    Adrien Burlacot, Ousmane Dao, Pascaline Auroy, Stephan Cuiné, Yonghua Li-Beisson, Gilles Peltier
    bioRxiv 2021.02.25.432959; doi: https://doi.org/10.1101/2021.02.25.432959
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    Alternative electron pathways of photosynthesis drive the algal CO2 concentrating mechanism
    Adrien Burlacot, Ousmane Dao, Pascaline Auroy, Stephan Cuiné, Yonghua Li-Beisson, Gilles Peltier
    bioRxiv 2021.02.25.432959; doi: https://doi.org/10.1101/2021.02.25.432959

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